The URL can be used to link to this page

Home My WebLink AboutElizabeth Oreck 7.8.21 Attachment 3JAVMA, Vol 242, No. 10, May 15, 2013 Scientiﬁc Reports 1359 SMALL ANIMALSIt has long been an article of faith among veterinarians and canine professionals that dogs obtained as puppies from pet stores have a higher prevalence of health and be- havioral problems.1 However, there has been a dearth of empirical studies to support this notion. In a retrospective survey of the owners of 737 adult dogs, Jagoea found that dogs obtained from pet shops had a signiﬁcantly higher prevalence of owner-directed (dominance-type) aggres- sion and social fears (fear of strangers, children, and unfa- miliar dogs) than did dogs from 5 other sources: breeders, animal shelters, friends or relatives, found or rescued off the streets, and home bred (ie, bred and reared in the cur- rent owner’s home).2 However, the sample size of pet store dogs in that studya was small (n = 20). Bennett and Rohlf3 investigated the frequency of potential problematic behavior patterns as reported Differences in behavioral characteristics between dogs obtained as puppies from pet stores and those obtained from noncommercial breeders Franklin D. McMillan, DVM, DACVIM; James A. Serpell, PhD; Deborah L. Duffy, PhD; Elmabrok Masaoud, PhD; Ian R. Dohoo, DVM, PhD Objective—To compare the owner-reported prevalence of behavioral characteristics in dogs obtained as puppies from pet stores with that of dogs obtained as puppies from noncommercial breeders. Design—Cross-sectional study. Animals—Dogs obtained as puppies from pet stores (n = 413) and breeder-obtained dogs (5,657). Procedures—Behavioral evaluations were obtained from a large convenience sample of current dog owners with the online version of the Canine Behavioral Assessment and Re-search Questionnaire, which uses ordinal scales to rate either the intensity or frequency of the dogs’ behavior. Hierarchic linear and logistic regression models were used to analyze the effects of source of acquisition on behavioral outcomes when various confounding and intervening variables were controlled for. Results—Pet store–derived dogs received signiﬁcantly less favorable scores than did breeder-obtained dogs on 12 of 14 of the behavioral variables measured; pet store dogs did not score more favorably than breeder dogs in any behavioral category. Compared with dogs obtained as puppies from noncommercial breeders, dogs obtained as puppies from pet stores had signiﬁcantly greater aggression toward human family members, unfamil-iar people, and other dogs; greater fear of other dogs and nonsocial stimuli; and greater separation-related problems and house soiling. Conclusions and Clinical Relevance—Obtaining dogs from pet stores versus noncommer-cial breeders represented a signiﬁcant risk factor for the development of a wide range of un-desirable behavioral characteristics. Until the causes of the unfavorable differences detected in this group of dogs can be speciﬁcally identiﬁed and remedied, the authors cannot recom-mend that puppies be obtained from pet stores. (J Am Vet Med Assoc 2013;242:1359–1363) by owners in a convenience sample of 413 companion dogs, of which 47 were obtained from pet stores. Re- sults indicated that dogs purchased from pet shops or shelters were considered by their owners to be more unfriendly or aggressive than were dogs purchased from breeders and signiﬁcantly more nervous than dogs bred by the present owner. However, by using broadly de- ﬁned behavioral subscales rather than discrete behav- iors, the researchers were not able to ascertain whether pet shop dogs had speciﬁc problematic behaviors more frequently than did dogs from other sources. Mugford4 reported analyzing a sample of 1,864 dogs with various behavioral problems and determined that “only 10% of purebred dogs obtained directly from breeders presented separation-related problems, where- as 55% of purebred dogs originating from so-called ‘puppy farms’ or ‘puppy mills’ present such problems.” Sample sizes and the way in which it was determined From the Best Friends Animal Society, 5001 Angel Canyon Rd, Kanab, UT 84741 (McMillan); the Department of Clinical Studies-Phila- delphia, School of Veterinary Medicine, University of Pennsylva- nia, Philadelphia, PA 19104 (Serpell, Duffy); and the Department of Health Management, Atlantic Veterinary College, University of Prince Edward Island, Charlottetown, PE C1A 4P3, Canada (Masaoud, Dohoo). Supported by a grant from the Animal Welfare Trust. Address correspondence to Dr. McMillan (dr.frank@bestfriends.org). ABBREVIATIONS C-BARQ Canine Behavioral Assessment and Research QuestionnaireCBE Commercial breeding establishmentNCB Noncommercial breeder 1360 Scientiﬁc Reports JAVMA, Vol 242, No. 10, May 15, 2013SMALL ANIMALSthat the dogs came from puppy farms or puppy mills were not reported. Some inconsistent ﬁndings have also been reported. Pierantoni et al5 compared owner-reported behaviors be- tween 70 adult dogs separated from their litters at 30 to 40 days of age and 70 adult dogs separated from their litters at 2 months of age. Their analysis included the source of the dog classiﬁed into 3 categories: breeder, pet shop, or friend or relative. The researchers found no sig- niﬁcant association between the source of the dog and the behavioral categories examined. In a study of the efﬁcacy of a dog-appeasing pheromone in reducing stress associ- ated with social isolation in puppies recently acquired from pet stores, Gaultier et al6 noted that their data did not seem to support the hypothesis that puppies from pet stores constitute a special, at-risk population for the development of behavioral problems. The researchers re- ported that the puppies in that study6 (n = 66) did not appear to disturb their owners any more than those in a previous study by Taylor and Mills7 involving puppies acquired from local pedigree dog breeders. However, the breeders in the latter study7 included a semicommercial breeder and at least 1 puppy mill.b Most puppies sold by pet stores in the United States are purchased from brokers, who may themselves be breeders but overwhelmingly acquire their puppies from high-volume breeding facilities, or CBEs, located throughout the United States.8 Conditions in the CBEs, which supply tens of thousands of puppies to retail pet stores each year, vary widely. Conditions in CBEs range from modern, clean, and well-kept to squalid, noxious, and gravely detrimental to animal health and welfare.9–11 The purpose of the study reported here was to eval- uate the hypothesis that dogs obtained as puppies from pet stores would be reported to have an increased prev- alence of behavioral problems, compared with dogs ob- tained as puppies from NCBs. Materials and Methods Data collection—Behavioral evaluations of the dogs were obtained by use of the online version of the C-BARQ, a standardized survey instrument with es- tablished reliability and validity characteristics.12 The C-BARQ is designed to provide quantitative assessments of a wide array of behavioral characteristics of dogs and has been widely used as a research tool for comparing behavior in different dog populations.13–15 The question- naire consists of 100 items that ask respondents to in- dicate on a series of 5-point ordinal rating scales their dogs’ typical responses to a variety of everyday situations during the recent past. The scales rate either the intensity (aggression, fear, and excitability subscales) or frequency (all remaining subscales and miscellaneous items) of the behaviors, with a score of 0 indicating the absence of the behavior and a score of 4 indicating the most intense or frequent form of the behavior. The C-BARQ currently comprises 14 behavioral factors or subscales and a fur- ther 22 miscellaneous stand-alone items. Higher scores are generally less favorable for all items and subscales, with the exception of trainability, for which higher scores are more desirable. Owners were also asked to indicate the dog’s current age at the time the survey was com- pleted, whether there were other dogs living in the same household, and whether the dog was used for speciﬁc working or recreational roles, including breed- ing or showing, ﬁeld trials or hunting, other sports (eg, agility, racing, or sledding), and working roles (eg, search and rescue, service, or sheep herding). To obtain information on the source from which the dog was acquired, owners were also asked to respond to the question, “where did you acquire this dog?” Possible responses included the following: bred him/her myself; from a breeder; from a shelter or rescue group; from a neighbor, friend, or relative; bought from a pet store; adopted as a stray; and other. Consistent with the 2 pre- vious studies3,a that offered pet-owning participants the choice of breeder as the source of the dog, the question in the C-BARQ regarding the source of the dog does not deﬁne the term breeder. Sample—The online C-BARQ was advertised originally via an article in the newsmagazine of the Vet- erinary Hospital of the University of Pennsylvania and by notices sent to Philadelphia-area veterinary clinics and the top 20 US breed clubs, as determined on the basis of American Kennel Club registrations. Availabil- ity of the survey then spread via word of mouth. No geographic limitations were applied, and participation included residents of the United States as well as other countries. A subset of these data consisting entirely of pet dogs whose owners reported obtaining them either from breeders (n = 5,657) or pet stores (413) was used for analysis. Breeder-obtained dogs were selected as the comparison group for the following reasons: age at the time of acquisition would most closely match pet store– obtained dogs; for the most part, breeder-obtained dogs are purebred as are those from pet stores; and the life history of the dog prior to purchase in breeder-obtained puppies is relatively standardized, thereby reducing the amount of environmental variability among the dogs of this group. These assumptions apply to the United States and may have less validity in other countries. Statistical analysis—Two-level hierarchic linear or logistic regression models were used to analyze the data on behavioral measures.16 The outcome variables (at- tachment and attention seeking, chasing, trainability, excitability, and energy) in the hierarchic linear model were treated as normally distributed continuous vari- ables. All other behavioral variables were dichotomized (eg, 0 or > 0) because they were typically highly skewed and it was impossible to identify a suitable transfor- mation method to normalize their distribution. These were analyzed with 2-level mixed logistic models. Both types of model aimed to assess the relationship between source of acquisition (eg, pet store vs breeder) and be- havior while controlling for various confounding vari- ables (other dogs in household, working or recreational roles, sex, and body weight) or intervening variables (neutered vs sexually intact and age at the time of eval- uation). All possible 2-way interactions between source of acquisition and confounding and intervening vari- ables were explored and accounted for in the modeling process. Nonsigniﬁcant confounding and intervening variables and interaction effects were removed from the JAVMA, Vol 242, No. 10, May 15, 2013 Scientiﬁc Reports 1361 SMALL ANIMALSmodel. Breed was also included in both models as a ran- dom effect to account for clustering of dogs at the breed level. Linear and logistic models were ﬁt via restricted and full maximum likelihood estimation procedures. The analysis was performed with statistical software17 by use of subject-speciﬁc models.c,d For all compari- sons, a value of P < 0.05 was considered signiﬁcant. Results According to the results of the multiple regression analyses, dogs acquired from pet stores differed signiﬁ- cantly from those acquired from breeders on 12 of 14 of the C-BARQ behavioral subscales. In no category did pet store dogs have a more desirable score than breeder dogs (Tables 1 and 2). The strongest effects were observed in relation to aggressive behavior. For example, sexu- ally intact pet store dogs were 3 times as likely to have owner-directed aggression as were sexually intact dogs acquired from breeders, and pet store dogs were near- ly twice as likely to have aggression toward unfamiliar dogs (dog-directed aggression). Pet store dogs were also 30% to 60% more likely to have stranger-directed aggres- sion, aggression to other household dogs, fear of dogs and nonsocial stimuli, separation-related problems, and touch sensitivity. In addition, they were somewhat more excitable, energetic, and attention seeking and generally less trainable, although this was only true for dogs that did not participate in working or recreational activities. The only C-BARQ subscales that were not signiﬁcantly different between pet store and breeder-derived dogs were chasing and stranger-directed fear. In addition, pet store–obtained dogs had a range of miscellaneous behav- ioral problems at signiﬁcantly higher frequencies than did those acquired from breeders (eg, escaping from the home, sexual mounting of people and objects, and most forms of house-soiling). Discussion Results of this study supported the view that dogs obtained as puppies from pet stores are more likely to develop behavioral problems as adults, compared with dogs obtained from NCBs. The retrospective nature of the data used in this analysis did not permit determina- tions of causality. However, there are several potential explanations for the differences between pet store and NCB dogs. Other variablesVariable controlled Predictor Effect 95% CI P value Excitability 1,2,3,4,6 PS 0.204 0.12 to 0.29 < 0.001Energy 1,2,3,4,6 PS 0.109 0.004 to 0.21 0.043Chasing PS 0.002 –0.13 to 0.10 0.769Attachment and 1,2,3,4,5,6 PS 0.204 0.12 to 0.29 < 0.001 attention seekingTrainability 1,2,3,4,5,6 PS–Not working dog –0.195 –0.26 to –0.13 < 0.001 PS– Working dog 0.098 –0.07 to 0.27 0.262 PS = Acquired from pet store.Other variables controlled were as follows: 1 = other dogs, 2 = dogs with working or recreational roles, 3 = sex, 4 = weight, 5 = neutered, 6 = age at time of evaluation (nonsigniﬁcant intervening variables [those variables that intervene the relationship between variable and predictor] were removed from the analyses). Table 1—Results of linear regression models comparing behavioral variables in dogs obtained from pet stores versus dogs obtained from NCBs. Other variablesVariable controlled Predictor OR 95% CI P value Separation-related behavior 1,2,3,4,5,6 PS 1.58 1.19–2.11 0.002Owner-directed aggression 1,2,3,4,5,6 PS–Not neutered 3.13 1.87–5.23 < 0.001 1,2,3,4,5,6 PS–Neutered 1.54 1.16–2.06 0.003Stranger-directed aggression 1,2,3,4,5,6 PS 1.59 1.18–2.16 0.003Nonsocial fear 1,2,3,4,5 PS 1.44 1.01–2.07 0.047Dog rivalry 1,2,3,4,6 PS 1.35 1.05–1.74 0.021Dog-directed fear 1,2,3,4,5 PS 1.33 1.03–1.71 0.030Dog-directed aggression 1,2,3,4,5,6 PS 1.96 1.44–2.67 < 0.001Touch sensitivity 1,2,3,4,5,6 PS 1.58 1.18–2.11 0.002Escapes from home or yard 1,2,3,4,5,6 PS 4.14 1.75–9.83 0.001Rolls in odorous material PS 0.86 0.67–1.09 0.214Coprophagia 1.08 0.86–1.36 0.502Chews objects 1.07 0.84–1.36 0.590Mounts objects or people 1,2,3,4,5 1.39 1.1–1.75 0.006Urinates against objects 1,2,3,4,5,6 PS 1.77 1.32–2.39 < 0.001 or furnishingsSubmissive urination 1,2,3,4,5,6 PS 1.53 1.13–2.07 0.007Urinates when left alone 1,2,3,4,5,6 PS 1.96 1.52–1.52 < 0.001Defecates when left alone 1,2,3,4,5 PS 1.68 1.31–2.16 < 0.001 See Table 1 for key. Table 2—Results of logistic regression models comparing behavioral variables in dogs obtained from pet stores versus dogs obtained from NCBs. 1362 Scientiﬁc Reports JAVMA, Vol 242, No. 10, May 15, 2013SMALL ANIMALSThe formative stages of the puppy’s life in the CBE are periods where stress may exert an impact on brain development. Although no studies on sources of stress in CBEs or their potential effects on the well-being of the dogs have been published, sources of stress have been in- vestigated in dogs living in conﬁnement in kennels,18–21 animal shelters,22,23 and laboratories.24,25 Similar stressors have been documented in the CBE environment,10 and it is therefore reasonable to suggest that the effects applied also to the dogs in the present study, despite some differ- ences in background, housing, and husbandry. Speciﬁc factors that have been determined to be associated with stress in dogs living in conﬁned environments include spatial restriction,18,19,23 extreme temperatures,9,26 aver- sive interactions with kennel staff,26,27 lack of perceived control or the capacity to avoid or regulate exposure to aversive stimuli,20–23 and limited access to positive hu- man and conspeciﬁc social interactions.18,24,25 A recent study11 on the mental health of dogs formerly used as breeding stock in CBEs found severe and long-lasting ad- verse effects in dogs living in this type of environment, offering evidence of the magnitude of stressors in CBEs. The stressors in the CBE environment may have acted at 2 stages of the developing puppies’ lives: the prenatal period and the ﬁrst 8 weeks after birth. A large body of research in humans and other animals has con- vincingly determined that prenatal stress (ie, stress ex- perienced by a pregnant female) causes alterations to the hypothalamic-pituitary-adrenal axis of the develop- ing fetus that may manifest later in life as an impaired ability to cope with stress,22 abnormal social behav- ior,28,29 and increased emotionality and fear-related be- havior.30 All of these outcomes are consistent with the differences detected in pet store– versus NCB-obtained dogs (ie, increased aggression, fear of dogs and nonso- cial stimuli, and excitability). Substantial evidence in humans and other animals indicates that stressful ex- periences in early life may have extensive and enduring effects with strong correlations to later development of behavioral abnormalities and psychopathologic abnor- malities.31–35 In dogs, Fox and Stelzner36 detected a short period at approximately 8 weeks of age when puppies are hypersensitive to distressing psychological or physical stimuli and during which a single unpleasant experience could result in long-term aversive or abnormal effects. Transport-related stress was suggested by both Mugford4 and Gaultier et al6 to be a potentially critical factor in the early lives of puppies from CBEs as they are shipped to pet stores throughout North America. Mugford,4 Serpell and Jagoe,2 and Bennett and Rohlf3 have each suggested that a reason for pet store and CBE puppies to have a high preva- lence of behavioral problems later in life is inadequate ear- ly socialization. In addition, genetic inﬂuences may play a role in the differences between pet store and NCB dogs, because a genetic basis for behavioral traits in dogs is con- sistent with ﬁndings observed in dogs of the present study, including fear, aggression, emotional reactivity, and non- speciﬁc alterations in temperament and personality.27,37,38 The reported differences in the 2 groups of dogs in the present study could be attributable to a number of owner-related factors. It is possible that people who buy puppies from pet shops may use different degrees or methods of training than people who buy puppies from an NCB. The importance of training in the devel- opment of problem behaviors was recently elucidated in the study3 of the relationship of potentially problematic behaviors with other variables. The researchers found that for the 5 behavioral subscales, the strongest predic- tor for scoring undesirably in 3 of the 5 subscales was the level of training the dog received. The present study did not attempt to collect demographic or background information on the dog owners; therefore, the degree to which such factors may have contributed to the ﬁnd- ings could not be assessed. An additional owner-related consideration is that it is possible that people who buy puppies from pet stores simply report potentially prob- lematic behaviors more readily than do others, irrespec- tive of the dog’s actual behavior. The data support the notion that dogs obtained as puppies from pet stores have substantial adverse behav- ioral differences, compared with dogs obtained from NCBs. Taken individually, however, the speciﬁc factors that differ between the 2 groups are not readily attrib- utable to a single deﬁnitive explanation. For example, stranger-directed aggression may be attributable to inad- equate socialization, maltreatment by humans, genetic factors, and prenatal stress. Taken collectively, no single explanatory factor appears capable of accounting for the differences between the 2 groups. For example, although inadequate socialization may explain increased aggres- sion, the most prominent emotional consequence of in- sufﬁcient socialization is fear,27,39 and whereas aggression toward humans (owners and unfamiliar people) was in- creased, fear toward humans was not. There were a number of limitations to the present study. The sample of dog owners was self-selected and therefore a potential source of bias. The question in the C-BARQ regarding the source of the dogs did not de- ﬁne breeder, leaving the participants to deﬁne the term for themselves. Accordingly, a breeder source could have indicated either type of NCB (hobby breeder or backyard breeder), and the level and type of care differ between the 2 types. These differences are presumably minor in comparison to the differences between NCBs and CBEs. It is also conceivable that the source of some dogs speciﬁed by the owner as breeder was a CBE; how- ever, it is reasonable to conclude that there would be no overlap between breeder and pet store categories (ie, no owner with a dog coming from a pet store would select breeder as a source, and no owner with a dog coming from a breeder would select pet store as a source). Results of the present study indicated that com- pared with dogs obtained as puppies from NCBs, dogs obtained as puppies from pet stores had signiﬁcantly greater aggression toward human family members, un- familiar people, and other dogs; fear of other dogs and nonsocial stimuli; separation-related problems; and urination and defecation problems in the home. On al- most all behavioral variables measured, pet store dogs received less favorable scores than breeder-obtained dogs. The diversity of behavioral differences between pet store–obtained and breeder-obtained dogs suggests a multifactorial cause and, accordingly, a multifactorial approach to correction; however, the data did not per- mit determination of the speciﬁc contributory factors and the degree of inﬂuence they exerted. In addition, JAVMA, Vol 242, No. 10, May 15, 2013 Scientiﬁc Reports 1363 SMALL ANIMALSbecause we did not compare the 2 groups of dogs in this study with other sources of dogs, the results should not be interpreted as an endorsement of any particular source of dogs. On the basis of these ﬁndings combined with earlier ﬁndings regarding pet store–obtained dogs, until the causes of the unfavorable differences detected in this group of dogs can be speciﬁcally identiﬁed and remedied, we cannot recommend that puppies be ob- tained from pet stores. a. Jagoe JA. Behaviour problems in the domestic dog: a retrospective and prospective study to identify factors inﬂuencing their develop- ment. PhD thesis, University of Cambridge, Cambridge, Eng- land, 1994. b. Taylor K, Senior Science Advisor, Secretariat to the Interna- tional Council for Animal Protection in Pharmaceutical Pro- grames (ICAPPP), British Union for the Abolition of Vivisection (BUAV), 16a Crane Grove, London, England: Personal commu- nication, 2011. c. xtmixed, Stata Statistical Software, release 11, StataCorp, College Station, Tex. d. xtmelogit, Stata Statistical Software, release 11, StataCorp, College Station, Tex. References 1. Fumarola AJ. With best friends like us who needs enemies? The phenomenon of the puppy mill, the failure of legal regimes to manage it, and the positive prospects of animal rights. Buffalo Environ Law J 1999;6:253–289. 2. Serpell J, Jagoe JA. Early experience and the development of be- havior. In: Serpell J, ed. The domestic dog: its evolution, behavior and interactions with people. Cambridge, England: Cambridge University Press, 1995;79–102. 3. Bennett PC, Rohlf VI. Owner-companion dog interactions: rela- tionships between demographic variables, potentially problem- atic behaviors, training engagement and shared activities. Appl Anim Behav Sci 2007;102:65–84. 4. Mugford RA. Canine behavioral therapy. In: Serpell J, ed. The do- mestic dog: its evolution, behavior and interactions with people. Cam- bridge, England: Cambridge University Press, 1995;139–152. 5. Pierantoni L, Albertini M, Pirrone F. Prevalence of owner- reported behaviors in dogs separated from the litter at two dif- ferent ages. Vet Rec 2011;169:468–474. 6. Gaultier E, Bonnafous L, Vienet-Legue D, et al. Efﬁcacy of dog- appeasing pheromone in reducing stress associated with social isolation in newly adopted puppies. Vet Rec 2008;163:73–80.7. Taylor K, Mills DS. A placebo-controlled study to investigate the effect of dog appeasing pheromone and other environmen- tal and management factors on the reports of disturbance and house soiling during the night in recently adopted puppies (Ca- nis familiaris). Appl Anim Behav Sci 2007;105:358–368. 8. Hunte Corp. Available at: www.huntecorp.com. Accessed Jun 5, 2011. 9. USDA. Final rules: animal welfare; 9 CFR parts 1 and 2. Avail- able at: www.nal.usda.gov/awic/pubs/Legislat/awaﬁn.shtml. Ac- cessed Jun 4, 2011. 10. USDA. Animal welfare reports and electronic freedom of informa- tion frequent requests. Available at: www.aphis.usda.gov/animal_ welfare/efoia. Accessed Feb 8, 2012. 11. McMillan FD, Duffy DL, Serpell JA. Mental health of dogs for- merly used as ‘breeding stock’ in commercial breeding establish- ments. Appl Anim Behav Sci 2011;135:86–94. 12. Hsu Y, Serpell JA. Development and validation of a question- naire for measuring behavior and temperament traits in pet dogs. J Am Vet Med Assoc 2003;223:1293–1300. 13. Serpell JA, Hsu Y. Effects of breed, sex, and neuter status on trainability in dogs. Anthrozoos 2005;18:196–207. 14. Duffy DL, Hsu Y, Serpell JA. Breed differences in canine aggres- sion. Appl Anim Behav Sci 2008;114:441–460. 15. Van den Berg SM, Heuven HCM, Van den Berg L, et al. Evalu- ation of the C-BARQ as a measure of stranger-directed ag- gression in three common dog breeds. Appl Anim Behav Sci 2010;124:136–141. 16. Dohoo I, Martin W, Stryhn H. Veterinary epidemiologic research. 2nd ed. Charlottetown, PE, Canada: VER Inc, 2009. 17. StataCorp. Stata 11 base reference manual. College Station, Tex: Stata Press, 2009;242–278, 306–355. 18. Beerda B, Schilder MB, van Hooff JA, et al. Chronic stress in dogs subjected to social and spatial restriction. I. Behavioral re- sponses. Physiol Behav 1999;66:233–242. 19. Beerda B, Schilder MB, Bernadina W, et al. Chronic stress in dogs subjected to social and spatial restriction. II. Hormonal and immunological response. Physiol Behav 1999;66:243–254. 20. Stephen JM, Ledger RA. An audit of behavioral indicators of poor welfare in kenneled dogs in the United Kingdom. J Appl Anim Welf Sci 2005;8:79–96. 21. Taylor KD, Mills DS. The effect of the kennel environment on canine welfare: a critical review of experimental studies. Anim Welf 2007;16:435–447. 22. Tuber DS, Miller DD, Caris KA, et al. Dogs in animal shel- ters: problems, suggestions, and needed expertise. Psychol Sci 1999;10:379–386. 23. Wells DL, Graham L, Hepper PG. The inﬂuence of length of time in a rescue shelter on the behavior of kennelled dogs. Anim Welf 2002;11:317–325. 24. Hughes HC, Campbell S, Kenney C. The effects of cage size and pair housing on exercise of Beagle dogs. Lab Anim Sci 1989;39:302–305. 25. Hubrecht RC. A comparison of social and environmental en- richment methods for laboratory housed dogs. Appl Anim Behav Sci 1993;37:345–361. 26. Morgan KN, Tromborg CT. Sources of stress in captivity. Appl Anim Behav Sci 2007;102:262–302. 27. Scott JP, Fuller JL. Genetics and the social behavior of the dog. Chicago: University of Chicago Press, 1965. 28. Braastad BO. Effects of prenatal stress on behavior of offspring of laboratory and farmed mammals. Appl Anim Behav Sci 1998;61:159–180. 29. Clarke AS, Schneider ML. Prenatal stress has long-term effects on behavioral responses to stress in juvenile rhesus monkeys. Dev Psychobiol 1993;26:293–304. 30. Lehmann J, Stöhr T, Feldon J. Long-term effects of prenatal stress experience and postnatal maternal separation on emotionality and attentional processes. Behav Brain Res 2000;107:133–144. 31. Edwards VJ, Holden GW, Felitti VJ, et al. Relationship between multiple forms of childhood maltreatment and adult mental health in community respondents: results from the adverse child- hood experiences study. Am J Psychiatry 2003;160:1453–1460. 32. Ladd CO, Huot RL, Thrivikraman KV, et al. Long-term behav- ioral and neuroendocrine adaptations to adverse early experi- ence. In: Mayer EA, Saper CB, eds. Progress in brain research: the biological basis for mind body interactions. Amsterdam: Elsevier, 2000;81–103. 33. Gunnar M, Quevedo K. The neurobiology of stress and develop- ment. Annu Rev Psychol 2007;58:145–173. 34. Tanapat P, Hastings NB, Rydel TA, et al. Exposure to fox odor inhibits cell proliferation in the hippocampus of adult rats via an adrenal hormone-dependent mechanism. J Comp Neurol 2001;437:496–504. 35. Dettling AC, Feldon J, Pryce CR. Early deprivation and behav- ioral and physiological responses to separation/novelty in the marmoset. Pharmacol Biochem Behav 2002;73:259–269. 36. Fox MW, Stelzner D. Behavioral effects of differential early ex- perience in the dog. Anim Behav 1966;14:273–281. 37. Saetre P, Strandberg E, Sundgren PE, et al. The genetic contribu- tion to canine personality. Genes Brain Behav 2006;5:240–248. 38. Svartberg K. Breed-typical behavior in dogs—historical remnants or recent constructs? Appl Anim Behav Sci 2006;96:293–313. 39. Horwitz DF, Neilson JC. Blackwell’s ﬁve-minute veterinary con- sult clinical companion—canine and feline behavior. Ames, Iowa: Blackwell Publishing, 2007.